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51 Gubler, F. et al. (1995) Gibberellin-regulated expression of a myb gene in
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gene promoter. Plant Cell 7, 1879–1891
52 Gubler, F. et al. (1997) Cloning of a rice cDNA encoding a transcription
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53 Weston, K. (1998) Myb proteins in life, death and differentiation. Curr. Opin.
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54 Gubler, F. et al. (1999) Target genes and regulatory domains of the
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55 Raventos, D. et al. (1998) HRT, a novel zinc finger, transcriptional repressor
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56 Hoecker, U. et al. (1995) Integrated control of seed maturation and
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57 Rogers, J.C. and Rogers, S.W. (1992) Definition and functional implications
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58 Rogers, J.C. et al. (1994) The cis-acting gibberellin response complex in highpI
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59 Willmott, R.L. et al. (1998) DNase1 footprints suggest the involvement of at
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29, 691–702
P
ost-embryonic development in higher plants is characterized
by the reiterative formation of lateral organs from the
flanks of apical meristems1
. A shoot apical meristem (SAM)
is initially formed during embryogenesis, and derivatives of this
meristem give rise to the above-ground portion of the plant. The
SAM contains a population of pluripotent stem cells, which serve
three primary functions1–4
:
(1) Lateral organs, such as leaves, are produced from the
peripheral regions of the SAM.
(2) The basal regions of the SAM contribute to the formation of
the stem.
(3) The stem cells of the SAM must replenish those regions
from which cells have been recruited and maintain the pool
of stem cells required for further growth.
In general, we focus on SAMs in this review, although extrapolation
of concepts to other shoot meristems, such as flower
meristems, will be discussed when pertinent.
As a result of histological analyses the SAM has been subdivided
in two different manners. First, three distinct zones of the
SAM are defined by cytoplasmic densities and cell division rates:
the peripheral zone, the central zone and the rib zone1–4
(Fig. 1).
These three zones might represent a functional subdivision of the
SAM although direct evidence for this is lacking. Lateral organs
are produced from cells recruited from the peripheral zone
whereas stem tissue is derived from cells recruited from the rib
zone. The central zone acts as a reservoir of stem cells, which
replenish both the peripheral and rib zones, as well as maintaining
the integrity of the central zone. It should be noted that these cells
do not act as permanent initials, but rather their behavior is governed
in a position-dependent manner. Second, the SAM is also
composed of clonally distinct layers of cells5
(Fig. 1). The fact that
the peripheral and central zones, as well as the lateral organs produced,
contain cells from the three clonally distinct layers indicates
that communication between cell layers is required to
coordinate developmental processes5,6
. For example, leaves in
most eudicot species are composed of derivatives from the epidermal
layer (L1), the subepidermal layer (L2) and corpus (L3)6
. One
of the earliest markers of leaf initiation from the peripheral zone is
the periclinal cell divisions in specific regions in the L2. Cells in
the L1 and L3 adjust their growth accordingly, with the entire
region acting coordinately to produce a leaf primordium.
In this review, we discuss some recent advances in our understanding
of three aspects of meristem functioning: the origin of
the SAM during embryogenesis, the maintenance of the stem
cell population in the central zone, and the relationships between
lateral organ primordia and the meristems from which they are
produced. Several excellent reviews cover broader views of the
biology of the SAM (Refs 2–4).
Formation and maintenance
of the shoot apical meristem
John L. Bowman and Yuval Eshed
Development in higher plants is characterized by the reiterative formation of lateral organs
from the flanks of shoot apical meristems. Because organs are produced continuously
throughout the life cycle, the shoot apical meristem must maintain a pluripotent stem cell
population. These two tasks are accomplished within separate functional domains of the
apical meristem. These functional domains develop gradually during embryogenesis.
Subsequently, communication among cells within the shoot apical meristem and between the
shoot apical meristem and the incipient lateral organs is needed to maintain the functional
domains within the shoot apical meristem.
Alison Lovegrove and Richard Hooley* are at IACR-Long Ashton
Research Station, Dept of Agricultural Sciences,
University of Bristol, Long Ashton, Bristol, UK BS41 9AF.
*Author for correspondence (tel ϩ44 1275 392181;
fax ϩ44 1275 394281; e-mail richard.hooley@bbsrc.ac.uk).
Embryonic origin of the shoot apical meristem
The origin of the SAM during embryogenesis has been the subject
of controversial debate7,8
. The primary point of contention is
whether the cotyledons are formed from the SAM, or if the SAM
and cotyledons arise independently. Resolution of this question
has major implications, influencing ideas on the homology of
leaves and cotyledons. We will not attempt to resolve this question
here, but rather argue that the complex histology of the mature
SAM is built up gradually during embryogenesis.
Although the tunica–corpus structure, which is characteristic of
the SAM (Fig. 1), is not evident until the torpedo stage of embryogenesis
in Arabidopsis (well after the initiation of the coty-
ledons)8
, the apical histological zonation (Fig. 1) is visible before
cotyledon initiation in some species7
. This has led to competing
hypotheses: either the SAM is formed by the apical portion of the
globular embryo, or alternatively, the SAM is not formed until the
tunica–corpus structure is evident at the late-heart or earlytorpedo
stage of embryogenesis. Two recent studies9,10
have
addressed this issue using gene expression patterns as histological
markers to analyze the development of the apical portion
of the Arabidopsis embryo from the globular through the
torpedo stages. The primary conclusions from these studies
(Fig. 2) are that:
(1) The complex gene expression patterns (histology) of the
SAM develop gradually during embryogenesis.
(2) Both independent and interdependent relationships exist
among genes directing SAM establishment and maintenance.
(3) The apical portion of the globular embryo is divided into
domains, demarcated by gene expression patterns, with
distinct developmental fates.
One of the earliest genes expressed is WUSCHEL (WUS), whose
mature SAM expression is limited to a small group of cells underneath
the outer three layers (in the L3), but is first expressed in the
apical subepidermal cells at the 16-cell stage of embryogenesis11
.
The WUS expression pattern gradually becomes limited to deeper
regions of the SAM as it forms (Fig. 2), suggesting that cell–cell
interactions probably dictate the boundaries of its expression
domain. SHOOT MERISTEMLESS (STM), CUP-SHAPED
COTYLEDON2 (CUC2) and AINTEGUMENTA (ANT) are all first
expressed in the late globular embryo9,10
. By the early transition
stage the expression patterns of these genes divide the apical
portion of the embryo into three regions9,10
(Fig. 2):
• A central region destined to give rise to the SAM (STM
and CUC2).
• A peripheral region, which is further subdivided into (i) regions
that will produce cotyledons (ANT) and (ii) regions where
growth will be suppressed, which form the boundaries between
the cotyledons (STM, CUC2 and ANT).
Later during the heart stage, CUC2 expression becomes restricted
to the boundary regions between the cotyledons and the SAM
(Fig. 2) – this restriction is dependent upon STM activity10
.
Although CUC2 and STM have complementary expression patterns
in the mature SAM, they are expressed in overlapping
domains during embryogenesis. This implies that other factors are
involved in establishing the complementary expression patterns of
the two genes10
. CUC2, which acts redundantly with CUC1, is
proposed to have a role in the separation of organs from the meristem
and from each other12
, in a manner analogous to that of NO
APICAL MERISTEM in petunia13
.
By early heart stage, after cotyledon primordia have formed,
UNUSUAL FLORAL ORGANS (UFO) and CLAVATA1 (CLV1)
are activated in the L2 and L3 of the presumptive SAM (Ref. 9).
Although the function of UFO in the SAM is unknown, CLV1 acts
with CLV3 and WUS to maintain the integrity of the central zone.
Both initial UFO expression and maintenance of CLV1 expression
requires STM activity, implying that STM acts to initiate a developmental
program required to establish or maintain several components
of the SAM (Ref. 9), consistent with the loss-of-function
phenotype of stm mutants8
.
From these studies it is clear that the apical region of the globular
embryo is progressively subdivided during development,
and that the establishment of the functional regions of the SAM is
a gradual and dynamic process that occurs during embryonic
pattern formation. In general, it appears that the earliest acting
genes are required for establishment or maintenance of stem cell
fate or alternatively, repression of differentiation (e.g. WUS,
STM). Whereas genes whose expression is initiated later might be
involved in regulating the size of the central zone (e.g. CLV1).
Maintenance of the central zone
One striking property of SAMs is their ability to remain relatively
constant in size. For example, the SAM of a several-hundredyear-old
mountain ash (Sorbus aucuparia) does not differ significantly
in size from the SAM of its cognate sapling. This is all the
more remarkable considering the continual production of lateral
organs from the peripheral zones and the lack of cell lineage
restriction in determining cell fates3,14–16
. These properties suggest
that cells within the SAM must continually assess their positions
relative to others, and subsequently decide to divide, differentiate
or remain as they are. Failure to choose appropriately leads to
either an accumulation of cells within the SAM, or alternatively,
loss of cells from the SAM, which in turn eventually leads to a
failure of SAM maintenance. Several mutants accumulating too
many cells in the SAM have been identified in Arabidopsis, and
these mutants fall primarily into two classes. The clavata mutants
accumulate excess cells in the central zone17,18
. By contrast, organ
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trends in plant science
Reviews
March 2000, Vol. 5, No. 3
Fig. 1. Histology of the shoot apical meristem (SAM). (a) Lateral
organs are produced from cells recruited from the peripheral zone
(PZ), whereas the bulk of the stem is derived from cells recruited
from the rib zone (RZ; the outermost layers of the stem are derived
from the peripheral zone). The central zone (CZ) acts as reservoir
of stem cells, which replenishes both the peripheral and rib zones
as well as maintaining the integrity of the central zone itself. (b)
The SAM is composed of clonally distinct layers of cells. In the
SAMs of eudicot plants, there are typically three layers. However,
the SAMs of many monocots, including grasses, are composed of
only two layers. The epidermal layer (L1) forms one clone, its
integrity being maintained by the almost exclusively anticlinal orientations
of cell division within the layer. The subepidermal layer
(L2) also exhibits almost exclusive anticlinal orientations of cell
division, which maintain its clonal distinctness. The L1 and L2 are
collectively referred to as the tunica. Cells interior to the L2 constitute
the corpus (L3), in which various planes of cell division are
observed. FILAMENTOUS FLOWER (FIL) expression (brown
color) demarcates lateral organ anlagen in the peripheral zone and
the abaxial domains of leaf primordia in Arabidopsis37,38
.
(a) (b)
CZ
PZ PZ
L1
L2
L3
RZ
initiation is affected in the mgoun mutants, and the location of
accumulation of excess cells is not presently clear19
. Mutants of
both classes also appear to have enlarged rib zones17–19
.
Based on morphology, histology and gene expression patterns,
mutations in CLAVATA1 (CLV1) or CLV3 lead to an accumulation
of cells in the central zone17,18,20–22
. Such a phenotype could
either be because of an increase in cell division rates in the central
zone, or alternatively, a reduction in the rate of recruitment of
cells from the central zone to the peripheral zone. A reduction in
the rate of recruitment has been argued based on observations of
cell division rates in the central zone of SAMs in clv1 mutants22
.
In wild-type SAMs, cell division rates are slower in the central
zone than in the adjacent peripheral zone, whereas in clv1
mutants, cell division rates within the central zone of both inflorescence
meristems and meristems of seven-day-old seedlings
were measured to be lower than that of the wild-type central
zones22
. Although this would suggest that the accumulation of
cells in the central zone is caused by a reduction in the rate of cells
being recruited into the peripheral zone, a possible caveat is that
observations on already enlarged meristems could be misleading
because of developmental epistasis. That is, that the reduction
in cell division rates in mature inflorescence meristems might be
a consequence of earlier alterations in the functioning of the meristem.
A more conclusive experiment would be to analyze the
structure of the SAM late in embryogenesis before the production
of the first set of leaves. In this case, it is apparent that SAMs of
clv3 embryos contain many more cells that those of the wild
type18
. Likewise, slightly later in development, after the initiation
of the first pair of leaves, there are considerably more cells in clv1
and clv3 SAMs than in wild-type SAMs (Ref. 23). Although these
phenotypes could be caused by leaf anlagen initiation during
embryogenesis, the observation that clv mutants produce more
leaves per day23
suggests that the accumulation of cells in the
central zone in these mutants is probably caused by an increased
cell division rate in the central zone itself. Further studies are
needed to resolve this issue.
The converse phenotype, the inability to maintain a population
of stem cells in the central zone, has been described for plants with
mutations in the WUS gene24
. SAM’s can be initiated by WUS
mutants, but cells within these SAMs are recruited to form lateral
organs without replenishment of the stem cell population in the
central zone24
. Thus mutations in WUS and CLV1/CLV3 have
essentially opposite effects on the stem cell population of the central
zone, suggesting that these genes act in pathways to promote
and restrict cell division rates, respectively, within the central zone.
Genetic interactions, the expression patterns and nature of the
encoded gene products of CLV1, CLV3 and WUS has led to the
development of a model of their action (Fig. 3). CLV1, whose
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trends in plant science
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March 2000, Vol. 5, No. 3
Fig. 2. Expression patterns of genes directing the establishment and maintenance of the shoot apical meristem (SAM) form gradually during
embryogenesis. (a–f) Expression patterns of six genes: the upper panel depicts the expression in a frontal section9
of a late globular-transition stage
of embryogenesis and the lower panel shows expression in a vegetative SAM. WUSCHEL (WUS)11
, SHOOT MERISTEMLESS (STM)9,47
, CUPSHAPED
COTYLEDON2 (CUC2)10
and AINTEGUMENTA (ANT)9
are all expressed by the transition stage, whereas expression of CLAVATA1
(CLV1)9,20
and UNUSUAL FLORAL ORGANS (UFO)9,48
is not detected until the heart stage. The expression pattern shown for CUC2 in the vegetative
SAM is an extrapolation of its reported embryonic expression10
and that observed for NO APICAL MERISTEM (NAM)13
. PHANTASTICA
(PHAN)33
and FILAMENTOUS FLOWER (FIL)37,38
(brown staining in each of the vegetative SAM panels) also mark the lateral organ anlagen in
a manner similar to that of ANT1 (Refs 2,49). It should be noted that the expression patterns depicted here are extrapolated from different sections
and that the precise patterns might differ from those shown. In addition, only qualitative patterns are shown here, but quantitative variations might
be present as well. (g–k) Complex and dynamic subdivision of the apical portion of the embryo. STM expression is depicted in orange; CUC2
depicted in pink; ANT depicted in yellow; STM ϩ ANT depicted in red; STM ϩ UFO depicted in blue; STM ϩ CLV1 depicted in green; STM ϩ
CLV1 ϩ UFO depicted in purple. (g and h) Depiction of the globular stage embryo in which ANT is expressed around the periphery and STM is
expressed at the periphery between the cotyledon anlagen9
. By the early heart stage (i), STM expression is also expressed in the central region and,
along with UFO, marks the site of the presumptive SAM (Ref. 9). During the heart stage (j), CLV1 is expressed in the central region whereas UFO
is restricted to the margins of the central region9
. Although STM and CUC2 have similar expression patterns at the transition stage9,10
, during the
heart stage STM and CUC2 resolve to complementary patterns, with STM expressed in the central region (which will give rise to the SAM) and
CUC2 expressed at the boundaries between the SAM and the cotyledon primordia10
(k). (g–k) Adapted from Refs 9 and 10.
Trends in Plant Science
(a) (b) (c) (d) (e)
(g) (h) (i) (j) (k)
(f)
WUS STM CUC2 ANT CLV1 UFO
mRNA is present primarily in the L3 of the central zone
(its expression might also extend into the L2), encodes a leucinerich
repeat (LRR) receptor kinase20,21
. CLV3, whose mRNA is primarily
restricted to the L1 and L2 of the central zone, encodes a
small, putatively secreted protein21
. Because CLV1 and CLV3 are
proposed to act in a common pathway18
, they might act as a
receptor-ligand pair in a signal transduction cascade that restricts
cell division rates in the central zone21
. The limited expression
domains of CLV1 and CLV3 imply that these genes act non-cellautonomously
to regulate central zone size, and suggests that
extensive cell–cell signaling, both within and between zones in
the meristem, is required for the maintenance of SAM integrity.
WUS encodes a homeodomain transcription factor and WUS
mRNA is localized to the L3 of the central zone11
. It has been proposed
that WUS-expressing cells act as an organizing center, conferring
stem-cell identity to overlying neighboring cells11
in a
manner similar to that of the quiescent center in the root meri-
stem25,26
. Because wus mutations are epistatic to clv1 mutations24
,
the CLV1/CLV3 signaling pathway could potentially act to negatively
regulate the activity of WUS directly. Thus one possible
model is that WUS promotes stem cell fate non-cell autonomously
among cells of the central zone11
, and that the CLV1/CLV3 signaling
pathway dampens this promotion by restricting cell division
within the central zone17,18,20–22
.
However, several key questions remain. First, although CLV1/
CLV3 activity is mitigated by KAPP (Refs 27,28), acts through
a complex that includes a Rho GTPase (Ref. 29) and is likely to
be modulated by CLV2 [another LRR receptor-like protein that
might heterodimerize with CLV1 (Ref. 30)], the ultimate targets of
this signal transduction cascade are unknown. Could WUS itself
be a target? Second, how does expression of WUS in the L3 of the
central zone non-cell, autonomously influence cell division in
the overlying cells? Third, what is the significance of the dynamic
WUS expression pattern within the meristem11
? The pattern
correlates with the nature of primordia initiation by the meristem:
• Expression in the upper layers (L2 or uppermost L3) when
opposite or whorled primordia are formed (e.g. floral organs by
flower meristems).
• Expression deeper in the L3, when primordia are initiated in a
spiral manner (e.g. leaf initiation by mature vegetative meristems).
However, it is unclear if the changes in WUS expression are involved
in the alteration of phyllotaxy. Intriguingly, CLV1 expression also
appears to shift upward when organs are initiated in a whorled
manner by the flower meristems20
. Fourth, and perhaps more interestingly,
how is the relative activity of the CL1/CLV3 system regulated?
Because the extent of cell division required in the central
zone is profoundly influenced by the need to replenish the loss of
cells in the peripheral zone (associated with lateral organ formation),
these processes are likely to be intimately linked. One
attractive hypothesis is that lateral organ primordia communicate
their formation to the SAM, resulting in a replenishment of the
peripheral zone from cells ultimately derived from the central zone.
Regulation of meristem function by its lateral organ primordia
The effects of signals emanating from mature leaves on the fate of
the apical meristem are already part of botany textbooks.
Recently, two different approaches demonstrated that such effects
also occur during primordia initiation. First, the localized exogenous
application of the cell-wall-loosening protein EXPANSIN to
the organ anlage of live tomato apices promoted organ primordia
formation at the site of application31
. Moreover, altering the normal
positions of primordia initiation can influence the phyllotactic
pattern of primordia initiation, implying primordium–SAM
communication. Although the expression pattern of EXPANSIN
mRNA is correlated with the pattern of primordia initiation32
, it is
unclear whether the effects of ectopic EXPANSIN activity are
mediated via biochemical or biophysical effects33
, or a combination
of both.
Non-cell-autonomous relationships between the SAM and lateral
organ primordia have also been uncovered in studies of the
Antirrhinum mutation phantastica (phan)34,35
. PHAN, which
encodes a MYB-related protein, is expressed throughout lateral
organ primordia. However, when mutant plants are grown in nonpermissive
conditions they develop radialized leaves and arrested
SAMs (Ref. 35). The radial leaves of phan mutants appear to consist
predominantly of abaxial cell types34
. Thus, although PHAN is
expressed in lateral organ primordia and appears to promote adaxial
cell fate, it is required non-cell-autonomously to maintain a
functional apical meristem. By contrast, leaves of the Arabidopsis
semi-dominant mutant phabulosa-1d (phb-1d) are radial with
ubiquitous adaxial cell types36
. In phb-1d mutants, the apical meristem
is enlarged and axillary meristems are formed around the
entire circumference of the leaves. These observations led to the
proposal that adaxial cell fate promotes meristem formation36
.
Conversely, abaxial cell fate might be incompatible with meristem
maintenance. Consistent with this hypothesis is the failure
to maintain a functional meristem in phan mutants34,35
. Recently,
several members of the YABBY gene family have been
proposed to promote abaxial cell fate in lateral organs37–39
. Each
family member is expressed in the abaxial domains of one or more
113
trends in plant science
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March 2000, Vol. 5, No. 3
Fig. 3. Expression patterns of genes involved in maintaining the
integrity of the central zone. CLAVATA3 (CLV3) mRNA is
restricted to the epidermal layer (L1) and subepidermal layer (L2)
of the central zone21
, whereas CLV1 mRNA is detected in the corpus
(L3) of the central zone20
. During vegetative development
WUSCHEL (WUS) mRNA is restricted to a few cells within the L3,
below the uppermost layer of the L3 (Ref. 11). It has been proposed
that CLV3 acts as a secreted ligand for the CLV1 receptor,
and that this signaling is responsible for restricting the size of the
central zone20,21
. By contrast, WUS is required to maintain an active
central zone, possibly by non-cell autonomously conferring a stem
cell identity on cells overlying its expression domain11
. The relative
overlaps in expression of these three genes in this figure are
estimated based on comparisons of published data, although the
simultaneous detection of these genes might alter this view.
FILAMENTOUS FLOWER (FIL) expression demarcates lateral
organ anlagen in the peripheral zone.
CLV3
WUS
CLV1
FIL
above-ground lateral organs. Ectopic expression of either of two
members of the YABBY gene family, FILAMENTOUS FLOWER
(FIL) or YABBY3, throughout the plant at a low level results in
partial conversion of adaxial tissues into abaxial ones. However,
with higher levels of ectopic expression, plants produce only
abaxialized cotyledons and display meristem arrest37
. Because
YABBY gene family members appear to promote abaxial cell
fate37–39
, it suggests that abaxial cell fates and meristematic fates
are incompatible.
One speculative model consistent with the above observations
is that as cells are set aside to become lateral organ primordia in
the peripheral zone of the SAM. Signals from the SAM itself are
required for the specification of adaxial cell fate within the lateral
organ anlagen (Fig. 4). Subsequently, signals emanating from the
adaxial regions of emerging lateral organ primordia would stimulate
the SAM to replenish the peripheral zone depleted by the
recruitment of cells into the lateral organs36
. The nature of the proposed
signals and their mechanism of transduction are presently
an enigma and remain a challenge for the future.
Complexities of the relationships between SAMs and lateral
organs are further exposed by the analysis of the maize ortholog
of PHAN – ROUGH SHEATH2 (RS2)40,41
. Leaves of rs2 mutants
appear similar to gain-of-function alleles of the SAM-specific
KNOTTED class I genes42–44
. Indeed, several genes of that group
were shown to be misregulated in either phan or rs2 mutants40–42
,
leading to the concept that PHAN and RS2 might have different
functions in Antirrhinum and Zea leaves, respectively40,41
. Specifically
it was suggested that RS2 could be involved in establishing
the proximal–distal axis rather than the abaxial–adaxial axis in
developing leaves41
. However, the development of these two axes
might be linked and one consequence of severely abaxialized
lateral organs could be a concomitant loss of proximal–distal
development34,35,37
. Analysis of orthologous genes in other species
might be required to clarify this issue.
Conclusions
The primary theme from the three vignettes presented is that cells
within the SAM are constantly reassessing their positions and
fates with respect to their neighbors to ensure proper formation
and maintenance of the SAM. Thus, SAM formation and maintenance
are active processes, and it is likely that extensive communication
pathways exist within and between the classically
defined regions of the meristem, as well as between the SAM and
incipient lateral organ primordia. This view of the SAM is consistent
with position-dependent rather than lineage-dependent development.
Extensive communication pathways imply numerous
receptors and their corresponding ligands, or perhaps morphogens
as conduits for cells talking to their neighbors and beyond. Given
the many candidate molecules uncovered by the Arabidopsis
genome-sequencing project (such as Refs 45,46), a challenge for
the future is to identify specific components that mediate such
communication pathways, and elucidate their interactions in
developing plants.
Acknowledgements
We apologize to those researchers whose work we were unable to
cite because of space limitations. For those whose work is cited, we
assume full responsibility for any errors in interpretation or presentation.
Work in J.L.B.’s laboratory is supported by the National
Science Foundation, the US Dept of Agriculture (NRICGP), the
Dept of Energy (Division of Biosciences), and the Beckman
Foundation. Y.E. was partially supported by a postdoctoral
fellowship from BARD.
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March 2000, Vol. 5, No. 3
Fig. 4. Model for interactions between lateral organ primordia and
the apical meristem. Experiments in which incipient leaf primordia
were separated by incisions from the shoot apical meristem
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signal required for the proper abaxial–adaxial development of the
leaf because the isolated primordia developed into radially symmetric,
apparently abaxialized, organs50,51
(arrow 1). One interpretation
is that signals emanating from the apical meristem promote
adaxial cell fate, and in the absence of such signals, abaxial cell
fate is the default pattern of differentiation. The establishment of
the abaxial and adaxial domains occurs during the transition from
leaf anlagen to leaf primordium because older primordia can
develop autonomously into phenotypically normal leaves50,51
. The
suggestion that adaxial leaf fate has a positive influence on the
maintenance of the meristem (arrow 2) is supported by the phenotype
of the adaxialized phb-1d mutant, in which axillary meristems
are formed around the basal circumference of the radial
leaves and the apical meristem is itself enlarged36
. Thus, meristems
produce lateral organs that in turn stimulate meristem formation
or regeneration36
. The failure to maintain a functional
meristem when lateral organs are abaxialized is also consistent
with this proposed signaling34,35,37
. The nature of the proposed signals,
their transduction (e.g. via plasmodesmata52–54
or secreted
ligands) and the precise points of origin and perception (e.g. central
or peripheral zone) are presently an enigma. Approximate
boundaries of the central, peripheral and rib zones are shown in
blue. AN, leaf anlagen.
1
2
AN
115
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John L. Bowman* and Yuval Eshed are at the Section of Plant
Biology, UC Davis, Davis, CA 95616, USA.
*Author for correspondence (tel ϩ1 530 754 9652;
fax ϩ1 530 752 5410; e-mail jlbowman@ucdavis.edu).